Advertisement

Heterotrophic, Planktonic Bacteria and Cycling of Phosphorus

Phosphorus Requirements, Competitive Ability, and Food Web Interactions
  • Olav Vadstein
Part of the Advances in Microbial Ecology book series (AMIE, volume 16)

Abstract

As early as 1956, Rigler reported that heterotrophic bacteria were responsible for a large share of the uptake of inorganic phosphorus (P) in Toussant Lake (Rigler, 1956). Tracer experiments revealed that the bacteria sequestered two thirds of the phosphate, and Rigler stated that

if they [bacteria] take up small increments of phosphorus received from inflowing water or from marginal vegetation, [bacteria] may compete with algae for this essential element.… If, in this process, they utilize inorganic phosphate, they would reduce the amount of phosphate available to algae and thus reduce the amount of organic matter produced by algae, (p. 560)

Keywords

Specific Growth Rate Competitive Ability Heterotrophic Bacterium Growth Yield Bacterial Biomass 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ammerman J. W., and Azam F., 1991, Bacterial 5’-nucleotidease activity in estuarine and coastal marine waters: Characterization of enzyme activity, Limnol. Oceanogr. 36:1427–1436.Google Scholar
  2. Andersen, O. K.., Goldman, J. C, Caron D. A., and Dennett, M. R., 1986, Nutrient cycling in a microflagellate food chain: III. Phosphorus dynamics, Mar. Ecol. Prog. Ser. 31:47–55.Google Scholar
  3. Andersen, T., 1997, Pelagic nutrient cycles: Herbivores as sources and sinks (Ecological Studies Vol. 129). Springer, Berlin, Heidelberg, New York.Google Scholar
  4. Andersen, T., and Hessen, D. O., 1991, Carbon, nitrogen and phosphorus content of freshwater zoo-plankton, Limnol. Oceanogr. 36:807–814.Google Scholar
  5. Andersson, G., Berggren, H., Cronberg, G., and Gelin, C, 1978, Effects of planktivorous fish on organisms and water chemistry in eutrophic lakes, Hydrobiol. 59:9–15.Google Scholar
  6. Andersen, T., Schartau, A. K. L., and Paasche, E., 1991, Quantifying external and internal nitrogen and phosphorus pools, as well as nitrogen and phosphorus supplied through remineralization, in coastal marine plankton by means of a dilution technique, Mar. Ecol. Prog. Ser. 69:67–80.Google Scholar
  7. Andrews, J. A., and Harris, R. F., 1986, r- and K-selection and microbial ecology, Adv. Microb. Ecol. 9:99–147.Google Scholar
  8. Azam, F, Fenchel, T., Field, J. G., Gray, J. S., Meyer-Reil, L. A., and Thingstad, F, 1983, The ecological role of water-column microbes in the sea, Mar. Ecol. Prog. Ser. 10:257–263.Google Scholar
  9. Baines, S. B., and Pace, M. L., 1991, The production of dissolved organic matter by phytoplankton and its importance to bacteria: Patterns across marine and freshwater ecosystems, Limnol. Oceanogr. 36:1078–1090.Google Scholar
  10. Bell, R. T., and Kuparinen, J., 1984, Assessing phytoplankton and bacterioplankton production during early spring in Lake Erken, Appl. Environ. Microbiol. 48:1221–1230.Google Scholar
  11. Benndorf, J., 1987, Food web manipulation without nutrient control: A useful strategy in lake restoration? Schweiz. Z Hydrobiol. 49:238–248.Google Scholar
  12. Bergh, Ø., Børsheim, K. Y., Bratbak, G., and Heldal, M., 1989, High abundance of virus found in aquatic environments, Nature 340:467–468.Google Scholar
  13. Berman, T., 1985, Uptake of [32P]orthophosphate by algae and bacteria in Lake Kinneret, J. Plankton Res. 7:71–84.Google Scholar
  14. Billen G., Servais P., and Fontigny, A., 1988, Growth and mortality in bacterial population dynamics of aquatic environments, Ergeb. Limnol. 31:173–183.Google Scholar
  15. Bird, B. F, and Kalff, J., 1987, Bacterial grazing by planktonic lake algae, Science 231:493–495.Google Scholar
  16. Bjørnsen, P., 1986, Bacterioplankton growth yield in continuous seawater cultures, Mar. Ecol. Prog. Ser. 30:191–196.Google Scholar
  17. Bloem, J., Starink, M., Bär-Gilissen, M.-J. B., and Cappenberg, T. E., 1988, Protozoan grazing, bacterial activity, and mineralization in two-stage continuous cultures, Appl. Environ. Microbiol. 54:3113–3121.Google Scholar
  18. Børsheim, K. Y., 1984, Clearance rate of bacterial-sized particles by freshwater ciliates, measured with monodisperse, fluorescent latex beads, Oecologia 63:286–288.Google Scholar
  19. Børsheim, K. Y., and Myklestad, S., 1997, Dynamics of DOC in the Norwegian Sea inferred from monthly profiles collected during 3 years at 66 degrees N, 2 degrees E, Deep-Sea Res. 44:593–601.Google Scholar
  20. Børsheim, K. Y, and Olsen, Y, 1984, Grazing activities by Daphnia pulex on natural populations of bacteria and algae, Verh. Internat. Verein. Limnol. 22:644–648.Google Scholar
  21. Bratbak, G., 1985, Bacterial biovolume and biomass estimation, Appl. Environ. Microbiol. 49:1488–1493.Google Scholar
  22. Bratbak, G., Thingstad, E, and Heldal, M., 1994, Viruses and the microbial loop, Microb. Ecol. 28:209–221Google Scholar
  23. Brendelberger, H., and Geller, W., 1985, Variability of filter structure in eight Daphnia species: Mesh sizes and filtering areas, J. Plankton Res. 7:473–486.Google Scholar
  24. Carlson, C. A., Ducklow, H. W., and Michaels, A. E, 1994, Annual flux of dissolved organic carbon from the euphotic zone in the northwestern Saragasso Sea, Nature 371:405–408.Google Scholar
  25. Caron, D. A., and Goldman, J. C., 1990, Protozoa nutrient generation, in: Ecology of Marine Protozoa (G. M. Capriulo, ed.), Oxford University Press, New York, pp. 283–306.Google Scholar
  26. Cembella, A. D., Antia, N. J., and Harrison, P. J., 1984, The utilization of inorganic and organic phosphorus compounds as nutrients by eukaryotic microalgae: A multidisciplinary perspective: Part 1, CRC Crit. Rev. Microbiol 10:317–391.Google Scholar
  27. Chen, M., 1974, Kinetics of phosphorus absorption by Corynebacterium bovis, Microb. Ecol. 1:164–175.Google Scholar
  28. Chrzanowski, T. H., Sterner, R. W., and Elser, J. J., 1995, Nutrient enrichment and nutrient regeneration stimulate bacterioplankton growth, Microb. Ecol. 29:221–230.Google Scholar
  29. Cole, J. J., Findley, S., and Pace, M. L., 1988, Bacterial production in fresh and saltwater ecosystems: A cross-system overview, Mar. Ecol. Prog. Ser. 43:1–10.Google Scholar
  30. Coleman, J. E., 1987, Structure and function of alkaline phosphatase. Introduction, in: Phosphate Metabolism and Cellular Regulation in Microorganisms (A. Torriani-Gorini, F. G. Rothman, S. Silver, A. Wright, and E. Yagil, eds), American Society for Microbiology, Washington, DC, pp. 113–114.Google Scholar
  31. Copin-Montégut, G., and Avril, B., 1993, Vertical-distribution and temporal variation of dissolved organic-carbon in the north-western mediterranean-sea, Deep-Sea Res. 40:1963–1972.Google Scholar
  32. Coveney, M. E, and Wetzel, R. G., 1992, Effects of nutrients on specific growth rate of bacterioplankton in oligotrophic lake water cultures, Appl. Environ. Microbiol. 58:150–156.Google Scholar
  33. Currie, D. J., 1990, Large-scale variability and interactions among phytoplankton, bacterioplankton, and phosphorus, Limnol. Oceanogr. 35:1437–1455.Google Scholar
  34. Currie, D. J., and Kalff, J., 1984a, The relative importance of bacterioplankton and phytoplankton in phosphorus uptake in freshwater, Limnol. Oceanogr. 29:311–321.Google Scholar
  35. Currie, D. J., and Kalff, J., 1984b, A comparison of the abilities of freshwater algae and bacteria to acquire and retain phosphorus, Limnol. Oceanogr. 29:298–310.Google Scholar
  36. Currie, D. J., and Kalff, J., 1984c, Can bacteria outcompete phytoplankton for phosphorus? A chemostat test, Microb. Ecol. 10:205–216.Google Scholar
  37. Dicks, J. W, and Tempest, D. W., 1966, The influence of temperature and growth rate on the quantitative relationship between potassium, magnesium, phosphorus and ribonucleic acid of Aerobacter aerogenes growing in a chemostat, J. Gen. Microbiol. 45:547–557.Google Scholar
  38. Droop, M. R., 1968, Vitamin B12 and marine ecology IV The kinetics of uptake, growth and inhibition in Monochrysis lutheri, J. Mar. Biol. Assoc. U.K. 48:689–733.Google Scholar
  39. Droop, M. R., 1983, 25 years of algal growth kinetics. A personal view, Botan. Marina 26:99–112.Google Scholar
  40. Duarte, C. M., 1992, Nutrient concentration of aquatic plants: Patterns across species, Limnol Oceanogr. 37:882–889Google Scholar
  41. Ducklow, H. W., and Carlson, C. A., 1992, Oceanic bacterial production, Adv. Microb. Ecol. 12:113–181.Google Scholar
  42. Egli, T., 1995, The ecological and physiological significance of the growth of heterotrophic microorganisms with mixtures of substrates, Adv. Microb. Ecol. 14:305–386Google Scholar
  43. Elser, J. J., Stabler, L. B., and Hassett, R. P., 1995, Nutrient limitation of bacterial growth and rates of bacterivory in lakes and oceans: a comparative study, Aquat. Microb. Ecol. 9:105–110.Google Scholar
  44. Fenchel, T., 1982, Ecology of heterotrophic microflagellates. II. Bioenergetics and growth, Mar. Ecol. Prog. Ser. 8:225–231.Google Scholar
  45. Fenchel, T., 1984, Suspended marine bacteria as food source, in: Flows of Energy and Materials in Marine Ecosystems (M. J. R. Fasham, ed.), Plenum Press, New York, pp. 301–315.Google Scholar
  46. Fenchel, T., and Blackburn, T. H., 1979, Bacteria and Mineral Cycling, Academic Press, New YorkGoogle Scholar
  47. Ferrante, J. G., 1976, The characterization of phosphorus excretion products of a natural population of limnetic sooplankton, Hydrobiologia 50:11–15.Google Scholar
  48. Fuhrman, J. A., and Azam, F, 1982, Thymidine incorporation as a measure of heterotrophic bacterio-plankton in marine surface waters: Evaluation and field results, Mar. Biol. 66:109–120.Google Scholar
  49. Fuhs, G. W., Demerle, S. D., Canelli, E., and Chen, M., 1972, Characterization of phosphorus-limited algae, Am. Soc. Limnol. Oceanogr. Spec. Publ. 1:113–132.Google Scholar
  50. Garber, J. H., 1984, Laboratory study of nitrogen and phosphorus remineralization during the decomposition of coastal plankton and seston, Estuarine Coastal Shelf Sci. 18:685–702.Google Scholar
  51. Gotham, I. J., and Rhee, G-. Y., 1981, Comparative kinetic study of phosphate-limited growth and phosphate uptake in phytoplankton in continuous culture, J. Phycol. 17:257–265.Google Scholar
  52. Grenney, W. J., Bella, D. A., and Curl, H. C, 1973, A theoretical approach to interspecific competition in phytoplankton communities, Am. Nat. 107:405–425.Google Scholar
  53. Güde, H., 1985, Influence of phagotrophic processes on the regeneration of nutrients in two-stage continuous culture systems, Microb. Ecol. 11:193–204.Google Scholar
  54. Güde, H., 1989, The role of grazing on bacteria in plankton succession, in: Plankton Ecology: Succession in Plankton Communities (U. Sommer, ed.), Springer, Berlin, pp. 337–364.Google Scholar
  55. Güde, H., 1991, Participation of bacterioplankton in epilimnetic phosphorus cycles of Lake Constance, Verh. Int. Ver. Limnol. 24:816–820.Google Scholar
  56. Hagström, Å., Larsson, U., Hörstedt, P., and Normark, S., 1979, Frequency of dividing cells, a new approach to the determination of bacterial growth rates in aquatic environments, Appl. Environ. Microbiol. 37:805–812.Google Scholar
  57. Harold, F. M., 1966, Inorganic polyphosphates in biology: Structure, metabolism, and function, Bacteriol. Rev. 30:772–794.Google Scholar
  58. Healey, F. P., 1975, Physiological indicators of nutrient deficiency in algae, Environment Canada, Fisheries and Marine Service, Technicaly Report no. 585.Google Scholar
  59. Healey, F. P., 1980, Slope of the Monod equation as an indicator of advantage in nutrient competition, Microb. Ecol. 5:281–286.Google Scholar
  60. Heckey R. E., and Kilham, P, 1988, Nutrient limitation of the phytoplankton in freshwater and marine environments: A review of recent evidence on the effect of enrichment, Limnol. Oceanogr. 33:796–822.Google Scholar
  61. Heldal, M., and Bratbak, G., 1991, Production and decay of viruses in aquatic environments, Mar. Ecol. Prog. Ser. 72:205–212.Google Scholar
  62. Heldal, M., Norland, S., and Tumyr, O., 1985, X-ray Microanalytic method for measurement of dry matter and elemental content of individual bacteria, Appl. Environ. Microbiol. 50:1251–1257.Google Scholar
  63. Herbert, D., 1961, The chemical composition of microorganisms as a function of their environment, Symp. Soc. Gen. Microbiol. 11:391–416.Google Scholar
  64. Hessen, D. O., 1985a, Filtering structure and particle size selection in coexisting cladocera, Oecologia 66:368–372.Google Scholar
  65. Hessen, D. O., 1985b, The relation between bacterial carbon and dissolved humic compounds in oligotrophy lakes, FEMS Microb. Ecol. 31:215–223.Google Scholar
  66. Hessen, D. O., and Andersen, T., 1990, Bacteria as a source of phosphorus for zooplankton, Hydrobiologia 206:217–223.Google Scholar
  67. Hessen, D. O., Andersen, T., and Lyche, A., 1990, Carbon metabolism in a humic lake; pool sizes and cycling through zooplankton, Limnol. Oceanogr. 35:84–99.Google Scholar
  68. Hessen, D. O., Faafeng, B., and Andersen, T., 1992. Zooplankton contribution to particulate phosphorus and nitrogen in lakes, J. Plankton Res. 14:937–947.Google Scholar
  69. Hobbie, J. E., 1988, A comparison of the ecology of planktonic bacteria in fresh and salt water, Limnol. Oceanogr. 33:750–764.Google Scholar
  70. Hobbie, J. E., Daly, R. J., and Jasper, S., 1977, Use of Nuclepore filters for counting bacteria by fluorescence microscopy, Appl. Environ. Microbiol. 33:1225–1228.Google Scholar
  71. Hutchinson, G. E., 1961, The paradox of the plankton, Am. Nat. 95:137–145.Google Scholar
  72. Jansson, M., 1988, Phosphate uptake and utilization by bacteria and algae, Hydrobiologia 170:177–189.Google Scholar
  73. Jansson, M., 1993, Uptake, exchange, and excretion of orthophosphate in phosphate-starved Scenedesmus quadricauda and Pseudomonas K7, Limnol. Oceanogr. 38:1162–1178.Google Scholar
  74. Jansson, M., Blomqvist, P., Jonsson, A., and Bergström, A.-K., 1996, Nutrient limitation of bacterio-plankton, autotrophic and mixotrophic phytoplankton, and heterotrophic nanoflagellates in Lake Örträsket, Limnol. Oceanogr. 41:1552–1559.Google Scholar
  75. Johannes, R. E., 1965, Influence of marine protozoa on nutrient regeneration, Limnol. Oceanogr. 10:434–442.Google Scholar
  76. Johannes, R. E., 1968, Nutrient regeneration in lakes and oceans. Adv. Microbiol. Sea 1:203–313.Google Scholar
  77. Jonsson, P. R., 1986, Particle size selection, feeding rates and growth dynamics of marine planktonic oligotrichous ciliates (Ciliophora, Oligotrichina), Mar. Ecol. Prog. Ser. 33:265–277.Google Scholar
  78. Jürgens, K., and Güde, H., 1990, Incorporation and release of phosphorus by planktonic bacteria and phagotrophic flagellates, Mar. Ecol. Prog. Ser. 59:271–284.Google Scholar
  79. Kivi, K., Kaitala, S., Kuosa, H., Kuparinen, J., Leskinen, E., Lignell, R., Marcussen, B., and Tamminen, T, 1993, Nutrient limitation and grazing control of the Baltic plankton community during annual succession, Limnol. Oceanogr. 38:893–905.Google Scholar
  80. Kjeldgaard, N. O., and Kurland, C. G., 1963, The distribution of soluble and ribosomal RNA as a function of growth rate, J. Mol. Biol. 6:341–348.Google Scholar
  81. Korstad, J., 1983, Nutrient regeneration by zooplankton in southern Lake Huron, J. Great Lakes Res. 9:374–388.Google Scholar
  82. Koschel, R., 1980, Untersuchung zur Phosphateaffinität des planktons in der euphotischen Zone Von Seen, Limnologica (Berlin) 12:141–145.Google Scholar
  83. Kuenzler, E. J., and Ketchum, B. H., 1962, Rate of phosphorus uptake by Phaeodactylum tricornutum, Biol. Bull. Mar. Biol. Lab., Woods Hole 123:134–145.Google Scholar
  84. Kuparinen, J., and Heinänen, A., 1993, Inorganic nutrients and carbon controlled bacterioplankton growth in the Baltic sea, Estuarine, Coastal and Shelf Sci. 37:271–285.Google Scholar
  85. Lampert, W., 1978, Release of dissolved organic carbon by grazing zooplankton, Limnol. Oceanogr. 23:831–834.Google Scholar
  86. Lean, D. R. S., 1973a, Movement of phosphorus between its biologically important forms in lake water, J. Fish. Res. Board Can. 30:1525–1536.Google Scholar
  87. Lean, D. R. S., 1973b, Phosphorus dynamics in lake water, Science 179:678–680.Google Scholar
  88. Lean, D. R. S., 1984, Metabolic indicators for phosphorus limitation, Verh. Internat. Verein. Limnol. 22:211–218.Google Scholar
  89. Lean, D. R. S., and Nalewajko, C., 1976, Phosphate exchange and organic phosphorus excretion by freshwater algae, J. Fish. Res. Bd. Can. 33:1312–1323.Google Scholar
  90. Lee S., and Fuhrman, J. A., 1987, Relationship between biovolume and biomass of natural derived marine bacterioplankton, Appl. Environ. Microbiol. 53:1298–1303.Google Scholar
  91. Lehman, J. T., 1980, Release and cycling of nutrients between planktonic algae and herbivores, Limnol. Oceanogr. 25:620–632.Google Scholar
  92. Lugtenberg, B., 1987, The pho regulon in Escherichia coli, in: Phosphate Metabolism and Cellular Regulation in Microorganisms (A. Torriani-Gorini, F. G. Rothman, S. Silver, A. Wright, and E. Yagil, eds.), American Society for Microbiology, Washington, DC, pp. 1–2.Google Scholar
  93. Martinussen I., and Thingstad, T. E, 1987, Utilization of N, P and organic C by heterotrophic bacteria. II. A comparison of experiments and a mathematical model, Mar. Ecol Prog. Sen 37:285–293.Google Scholar
  94. Middelboe M., and Søndergaard, M., 1993, Bacterial growth yield: Seasonal variations and coupling to substrate lability and ß-glucosidase activity, Appl. Environ. Microbiol. 59:3916–3921.Google Scholar
  95. Monod, J., 1942, Recherches sur la Croissance des Cultures Bactériennes, Herman, Paris.Google Scholar
  96. Morel, E M. M., 1987, Kinetics of nutrient upt ake and growth in phytoplankton, J. Phycol. 23:137–150.Google Scholar
  97. Morris D. P., and Lewis Jr., W. M., 1992, Nutrient limitation of bacterioplankton growth in Lake Dillon, Colorado, Limnol. Oceanogr. 37:1179–1192.Google Scholar
  98. Neidhardt, E C, and Magasanik, B., 1960, Studies on the role of ribonucleic acid in the growth of bacteria, Biochim. Biophys. Acta 42:99–116.Google Scholar
  99. Neidhardt, F.C., Ingraham, J. L., and Schaechter, M., 1990, Physiology of the Bacterial Cell. A molecular approach, Sinauer Associates, Sunderland, Mass.Google Scholar
  100. Neijssel, O. M., and Tempest, D. W, 1976, Bioenergetic aspects of aerobic growth of Klebsiella aerogenes NCTC 418 in carbon-limited and carbon-sufficient chemostat culture, Arch. Microbiol. 107:215–221.Google Scholar
  101. Nielsen, M. V., and Olsen, Y., 1989, The dependence of the assimilation efficiency in Daphnia magna on the 14C-labelling period of the food algae Scenedesmus acutus, Limnol. Oceanogr. 34:1311–1315.Google Scholar
  102. Nissen, H., Heldal, M., and Norland, S., 1987, Effect of phosphate on growth response and elemental composition of Vibrio natriegens, Can. J. Microbiol. 33:583–588.Google Scholar
  103. Nordland, S., Heldal, M., and Tumyr, O., 1987, On the relation between dry matter and volume of bacteria, Microb. Ecol. 13:95–101.Google Scholar
  104. Nygaard, K., and Tobiesen, A., 1993, Bacterivory in algae: A survival strategy during nutrient limitation, Limnol. Oceanogr. 38:273–279.Google Scholar
  105. Olsen, Y, 1988, Phosphate kinetics and competitive ability of planktonic blooming cyanobacteria under variable phosphate supply, Dr. Techn. thesis, University of Trondheim, Trondheim, Norway.Google Scholar
  106. Olsen, Y, 1989, Evaluation of competitive ability of Staurastrum luetkemuellerii (Chlorophyceae) and Microcystis aeruginosa (Cyanophyceae) under P limitation, J. Phycol. 25:486–499.Google Scholar
  107. Olsen, Y, and Østgaard, K., 1985, Estimating release rates of phosphorus from zooplankton: Model and experimental verification, Limnol. Oceanogr. 30:844–852.Google Scholar
  108. Olsen, Y, and Vadstein, O., eds., 1989, NTNFs Research Program on Eutrophication, Final Report for Phase 1-3, 1978-1988, [In Norwegian] Tapir, Trondheim, NorwayGoogle Scholar
  109. Olsen, Y, Jensen, A., Reinertsen, H., Børsheim, Y, Heldal, M., and Langeland, A., 1986a, Dependence of the rate of release of phosphorus by zooplankton upon the P:C ratio in the food supply, as calculated by a recycling model, Limnol. Oceanogr. 31:34–44.Google Scholar
  110. Olsen, Y, Vårum, K. M., and Jensen, A., 1986b, Some characteristics of the carbon compounds released by Daphnia, J. Plankton Res. 8:505–517.Google Scholar
  111. Olsen, Y, Vadstein, O., Jensen, A., and Andersen, T., 1989, Competition between Staurastrum luetkemullerii (chlorophycae) and Microcystis aeruginosa (cyanophycae) under varying modes of phosphate supply, J. Phycol 25:499–508.Google Scholar
  112. Pace, M. L., and Funke, E., 1991, Regulation of planktonic microbial communities by nutrients and herbivores, Ecology 72:904–914.Google Scholar
  113. Pearl, H. W, and Lean, D. R. S., 1976, Visual observation of phosphorus movement between algae, bacteria and abiotic particles in lake waters, J. Fish. Res. Board Can. 33:2805–2813.Google Scholar
  114. Pengerud, B., Skjoldal, E. F., and Thingstad, T. F., 1987, The reciprocal interaction between degradation of glucose and ecosystem structure. Studies in mixed chemostat cultures of marine bacteria, algae, and bacterivorous nanoflagellates, Mar. Ecol. Prog. Sen 35:111–117.Google Scholar
  115. Peters, R., and Lean, D., 1973, The characterization of soluble phosphorus released by limnetic zoo-plankton, Limnol. Oceanogr. 18:270–279.Google Scholar
  116. Pirt, S. J., 1982, Maintenance energy: A general model for energy-limited and energy-sufficient growth, Arch. Microbiol. 133:300–302.Google Scholar
  117. Poindexter, J. S., 1981, Oligotrophy. Fast and famine existence, Adv. Microb. Ecol. 5:63–89.Google Scholar
  118. Reiners, W. A., 1986, Complementary models for ecosystems, Am. Nat. 127:59–73.Google Scholar
  119. Reinertsen, H., and Langeland, A., 1982, The effect of a lake fertilization on the stability and material utilization of a limnetic ecosystem, Holarctic Ecol. 5:311–324.Google Scholar
  120. Reinertsen, H., Koksvik, D., Langeland, A., and Olsen, Y., 1989, Effects of fish removal on the limnetic ecosystem in a eutrophic lake, Can. J. Fish. Aquat. Sci. 47:166–173.Google Scholar
  121. Rhee, G-Y., 1972, Competition between an alga and an aquatic bacterium for phosphate, Limnol. Oceanogr. 17:505–514.Google Scholar
  122. Rhee, G-Y, 1978, Effects of N:P atomic ratios and nitrate limitation on algal growth, cell composition, and nitrate uptake, Limnol. Oceanogr. 23:10–25.Google Scholar
  123. Rhee, G-Y, 1982, Effects of environmental factors and their interactions on phytoplankton growth, Adv. Microb. Ecol. 6:33–74.Google Scholar
  124. Riemann, B., 1985, Potential importance of fish predation and zooplankton grazing on natural populations of freshwater bacteria, Appl. Environ. Microbiol. 50:187–193.Google Scholar
  125. Riemann, B., and Søndergaard, M., eds., 1986, Carbon Dynamics in Eutrophic, Temperate Lakes, Elsevier, New YorkGoogle Scholar
  126. Rigler, F. H., 1956, A tracer study of the phosphorus cycle in lake water, Ecology 37:550–562.Google Scholar
  127. Rigler, F H., 1973, A dynamic view of the phosphorus cycle in lakes, in: Environmental phosphorus handbook E E. J. Griffith, A. Beeton, J. M. Spencer, and D. T. Mitchell, (eds.), John Wiley&Sons, New York, pp. 539–572.Google Scholar
  128. Robertson, B. R., and Button, D. K., 1979, Phosphate-limited culture of Rhodotorula rubra: Kinetics of transport, leakage, and growth, J. Bacteriol. 138:884–895.Google Scholar
  129. Robinson, J. D., Mann, K. H., and Novitsky, J. A., 1982, Conversion of the particulate fraction of seaweed detritus to bacterial biomass, Limnol. Oceanogr. 27:1072–1079.Google Scholar
  130. Rosenberg, H., 1987, S. Silver, ed., Academic Press, London}, pp. 205–24Google Scholar
  131. Rosenberg, H., Gerdes, R. G., and Chegwidden, K., 1977, Two systems for the uptake of phosphate in Escherichia coli, J. Bacteriol. 131:505–511.Google Scholar
  132. Rosenberg H., Russel L. M., Jacomb P. A., and Chegwidden, K., 1982, Phosphate exchange in the Pit transport system in Escherichia coli, J. Bacteriol. 149:123–13Google Scholar
  133. Rosset R., Mien J., and Monier, R., 1966, Ribonucleic acid composition of bacteria as a function of growth rate, J. Mol. Biol. 18:308–320.Google Scholar
  134. Rothhaupt, K. O., 1992, Stimulation of phosphorus-limited phytoplankton by bacterivorous flagellates in laboratory experiments, Limnol. Oceanogr. 37:750–759.Google Scholar
  135. Rothhaupt K. O., and Güde, H., 1992, The influence of spatial and temporal concentration gradients on phosphate partitioning between different size fractions of plankton: Further evidence and possible causes, Limnol. Oceanogr. 37:739–749.Google Scholar
  136. Sakshaug E., and Olsen, Y, 1986, Nutrient status of phytoplankton blooms in Norwegian waters and algal strategies for nutrient competition, Can. J. Fish. Aquat. Sci. 43:389–396.Google Scholar
  137. Sakshaug E., Andresen K., Myklestad S., and Olsen, Y, 1983, Nutrient status of phytoplankton communities in Norwegian waters (marine, brackish, and fresh) as revealed by their chemical composition, j. Plankton Res. 5}:175–1Google Scholar
  138. Sanders R. W., and Porter, K., 1988, Phagotrophic phytoflagellates, Adv. Microb. Ecol. 10:167–192.Google Scholar
  139. Schwaerter S., Søndergaard M., Riemann B., and Jensen, L. M., 1988, Respiration in eutrophic lakes: The contribution of bacterioplankton and bacterial growth yield, J. Plankton Res. 10:515–531.Google Scholar
  140. Servais P., Billen G., and Rego, J. V., 1985, Rate of bacterial mortality in aquatic environments, Appl. Environ. Microbiol. 49:1448–1454.Google Scholar
  141. Sherr B. F., and Sherr, E. B., 1984, Role of heterotrophic protozoa in carbon and energy flow in aquatic ecosystems, in: Current Perspectives in Microbial Ecology (edM. J. Klug and C. A. Reddy}, eds.), American Society for Microbiology, Washington, DC, pp. 412–423.Google Scholar
  142. Sherr, B. R, Sherr, E. B., and Berman, T., 1982, Decomposition of organic detritus: A selective role for microflagellated protozoa, Limnol. Oceanogr. 27:765–769.Google Scholar
  143. Sherr B. P., Sherr E. B., and Fallon, R. D., 1987, Use of monodispersed, fluorescently labelled bacteria to estimate in situ protozoan bacterivory, Appl. Environ. Microbiol. 53:958–965.Google Scholar
  144. Shuter, B. J., 1978, Size dependence of phosphorus and nitrogen subsistence quotas in unicellular organisms, Limnol. Oceanogr. 23:1248–1255.Google Scholar
  145. Simon M., and Azam, R, 1989, Protein content and protein synthesis rates of planktonic marine bacteria, Mar. Ecol Prog. Ser. 51:201–213.Google Scholar
  146. Simon M., Cho, B. C, and Azam, R, 1992, Significance of bacterial biomass in lakes and the ocean: Comparison to phytoplankton biomass and biogeochemical implications, Mar. Ecol. Prog. Ser. 86:103–110.Google Scholar
  147. Smith, R. E. H., and Kalff, J., 1982, Size-dependent phosphorus uptake kinetics and cell quota in phytoplankton, J. Phycol. 18:275–284.Google Scholar
  148. Sommer, U., 1984, The paradox of the plankton: Fluctuations of the phosphorus availability maintain diversity of phytoplankton on flow-through cultures, Limnol. Oceanogr. 29:633–636.Google Scholar
  149. Sommer, U., 1985, Comparison between steady state and non-steady state competition: Experiments with natural phytoplankton, Limnol. Oceanogr. 30:335–346.Google Scholar
  150. Strayer, D., 1988, On the limits to secondary production, Limnol. Oceanogr. 33:1217–1220.Google Scholar
  151. Tarapchak S. J., and Moll, R. A., 1990, Phosphorus sources for phytoplankton and bacteria in Lake Michigan, J. Plankton Res. 12:743–758.Google Scholar
  152. Taylor, W. D., 1984, Phosphorus flux through epilimnetic zooplankton from Lake Ontario: Relationship with body size and significance to phytoplankton, Can. J. Fish. Aquat. Sci. 41:1702–1712.Google Scholar
  153. Taylor W. D., and Lean, D. R. S., 1991, Phosphorus pool sizes and fluxes in the epilimnion of a mesotrophic lake, Can. J. Fish. Aquat. Sci. 48:1293–1301.Google Scholar
  154. Terry K. R., and Hooper, A. B., 1970, Polyphosphate and orthophosphate content of Nitrosomonas europaes as a function of growth, J. Bacteriol. 103}:199–2Google Scholar
  155. Tezuka, Y., 1989, The C:N:P ratio of phytoplankton determines the relative amounts of dissolved inorganic nitrogen and phosphorus released during aerobic decomposition, Hydrobiologia 173:55–63.Google Scholar
  156. Tezuka, Y., 1990, Bacterial regeneration of ammonium and phosphate as affected by the carbon:nitrogen:phosphorus ratio of organic substrates, Microb. Ecol. 19:227–238.Google Scholar
  157. Thingstad, T. F, 1987, Analyzing the “microbial loop. ” Experimental and mathematical model studies of interactions between heterotrophic bacteria and their trophic neighbours in the pelagic food webs. Ph.D. thesis, University of Bergen, Berger, Norway.Google Scholar
  158. Thingstad T. F., and Pengerud, B., 1985, Fate and effect of allochthonous organic material in aquatic microbial ecosystems. An analysis based on chemostat theory, Mar. Ecol. Prog. Ser. 21:47–62.Google Scholar
  159. Thingstad, T. F, Havskum, H., Garde K., and Riemann, B., 1996, On the strategy of “eating your competitor ”: A mathematical analysis of algal mixotrophy, Ecology 77:2108–2118.Google Scholar
  160. Thingstad, T. F, Hagström, Å., and Rassoulzadegan, P., 1997, Accumulation of degradable DOC in surface waters: Is it caused by a malfunctioning microbial loop? Limnol. Oceanogr. 42:398–404.Google Scholar
  161. Thomas, E. A., 1973, Phosphorus and eutrophication, in: Environmental Phosphorus Handbook (E. J. Griffith, A. Beeton, J. M. Spencer, and D. T. Mitchell, eds.), John Wiley&Sons, New York, pp. 585–611.Google Scholar
  162. Tilman, D., 1977, Resource competition between planktonic algae: An experimental and theoretical approach, Ecology 58:338–348.Google Scholar
  163. Tilman, D., Kilham, S. S., and Kilham, P., 1982, Phytoplankton community ecology: The role of limiting nutrients, Annu. Rev. Ecol. Syst. 13:348–372.Google Scholar
  164. Toolan, T., Wehr, J. E., and Findlay, S., 1991, Inorganic phosphorus stimulation of bacterioplankton production in a meso-eutrophic lake, Appl. Environ. Microbiol. 57:2074–2078.Google Scholar
  165. Torriani-Gorini, A., Rothman, F. G., Silver, S., Wright, A., and Yagil, E., eds., 1987, Phosphate Metabolism and Cellular Regulation in Microorganisms, American Society for Microbiology, Washington, DC.Google Scholar
  166. Tsai, J. C, Aladegami, S. L., and Vela, G. R., 1979, Phosphate-limited culture of Azotobactervinilandii, J. Bacteriol. 139:639–64Google Scholar
  167. Vadstein, O., 1998, Evaluation of competitive ability of two heterotrophic planktonic bacteria under phosphorus limitation, Aquatic Microb. Ecol. 14:119–127.Google Scholar
  168. Vadstein, O., and Olsen, Y., 1989, Chemical composition and PO4 uptake kinetics of limnetic bacterial communities cultured in chemostat under P limitation, Limnol. Oceanogr. 34:939–946.Google Scholar
  169. Vadstein, O., Jensen, A., Olsen, Y, and Reinertsen, H., 1988, Growth and phosphorus status of limnetic phytoplankton and bacteria, Limnol. Oceanogr. 33:489–503.Google Scholar
  170. Vadstein, O., Harkjerr, B. O., Jensen, A., Olsen, Y, and Reinertsen, H., 1989, Cycling of organic carbon in the photic zone of a eutrophic lake with special reference to the bacteria, Limnol. Oceanogr. 34:840–855.Google Scholar
  171. Vadstein, O., Jensen, A., Olsen, Y, and Reinertsen, H., 1993, The role of planktonic bacteria in phosphorus cycling in lakes—Sink and link, Limnol. Oceanogr. 38:1539–1544.Google Scholar
  172. Vadstein, O., Brekke, O., Andersen, T., and Olsen, Y, 1995, Estimation of phosphorus release rates from natural zooplankton communities feeding on planktonic algae and bacteria, Limnol. Oceanogr. 40:250–262.Google Scholar
  173. Vollenweider, R. A., 1968, Scientific fundamentals of the eutrophication of lakes and flowing waters, with particular reference to nitrogen and phosphorus as factors in eutrophication, Technical Report DAS/CSI/68.27, Paris.Google Scholar
  174. Vollenweider, R. A., 1976, Advances in defining critical loading levels for phosphorus in lake eutrophication, Mem. Ist. Ital. Idrobiol. 33:53–83.Google Scholar
  175. Wang, L., Miller, T. D., and Priscu, J. C, 1992, Bacterioplankton nutrient deficiency in a eutrophic lake, Arch. Hydrobiol. 125:423–439.Google Scholar
  176. Wanlian, L., and Xinshou, L., 1985, Elementary composition of some dominant zooplankters in Lake Donghu, Wuhan, Acta Hydrobiol. Sinica 9:258–263.Google Scholar
  177. Wanner U. and Egli T 1990 Dynamics of microbial growth and cell composition in batch culture FEMS Microbiol. Rev. 7519–44Google Scholar
  178. Watson, S. W, Novitsky, T. J., Quinby, H. L., and Valois, F. W., 1977, Determination of bacterial number and biomass in the marine environment, Appl. Environ. Microbiol. 33:940–946.Google Scholar
  179. Wetzel, R. G., 1983, Limnology, 2nd ed., Saunders, Philadelphia.Google Scholar
  180. White, P. A., Kalff, J., Rasmussen, J. B., and Gasol, J. M., 1991, The effect of temperature and algal biomass on bacterial production and specific growth rate in freshwater and marine habitats, Microb. Ecol. 21:99–118.Google Scholar
  181. Wikner, J., Anderson, A., Normark, S., and Hagström, Å., 1986, Use of genetically marked minicells as a probe in measurements of predation on bacteria in aquatic environments, Appl. Environ. Microbiol. 52:4–8.Google Scholar
  182. Zimmermann, R., and Meyer-Reil, L.-A., 1974, A new method for fluorescence staining of bacterial populations on membrane filters, Kieler Meeresforschungen 30:24–27.Google Scholar
  183. Zweifel, U. L., Norrman, B., and Hagström, Å., 1993, Consumption of dissolved organic carbon by marine bacteria and demand for inorganic nutrients, Mar. Ecol. Prog. Sen 101:23–32.Google Scholar

Copyright information

© Springer Science+Business Media New York 2000

Authors and Affiliations

  • Olav Vadstein
    • 1
  1. 1.Trondhjem Biological StationNorwegian University of Science and TechnologyTrondheimNorway

Personalised recommendations